Ancient role of sulfakinin/cholecystokinin-type signalling in inhibitory regulation of feeding processes revealed in an echinoderm

Elife. 2021 Sep 7:10:e65667. doi: 10.7554/eLife.65667.

Abstract

Sulfakinin (SK)/cholecystokinin (CCK)-type neuropeptides regulate feeding and digestion in protostomes (e.g. insects) and chordates. Here, we characterised SK/CCK-type signalling for the first time in a non-chordate deuterostome - the starfish Asterias rubens (phylum Echinodermata). In this species, two neuropeptides (ArSK/CCK1, ArSK/CCK2) derived from the precursor protein ArSK/CCKP act as ligands for an SK/CCK-type receptor (ArSK/CCKR) and these peptides/proteins are expressed in the nervous system, digestive system, tube feet, and body wall. Furthermore, ArSK/CCK1 and ArSK/CCK2 cause dose-dependent contraction of cardiac stomach, tube foot, and apical muscle preparations in vitro, and injection of these neuropeptides in vivo triggers cardiac stomach retraction and inhibition of the onset of feeding in A. rubens. Thus, an evolutionarily ancient role of SK/CCK-type neuropeptides as inhibitory regulators of feeding-related processes in the Bilateria has been conserved in the unusual and unique context of the extra-oral feeding behaviour and pentaradial body plan of an echinoderm.

Keywords: Asterias rubens; evolutionary biology; feeding; neuropeptides; receptors; starfish; sulfakinin/cholecystokinin.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Asterias / genetics
  • Asterias / metabolism
  • Calcium-Calmodulin-Dependent Protein Kinases
  • Cell Line
  • Cholecystokinin / metabolism*
  • Cholecystokinin / pharmacology*
  • Echinodermata
  • Nervous System / metabolism
  • Neuropeptides / classification
  • Neuropeptides / genetics
  • Neuropeptides / metabolism
  • Phylogeny
  • Signal Transduction / drug effects*
  • Starfish

Substances

  • Neuropeptides
  • Cholecystokinin
  • Calcium-Calmodulin-Dependent Protein Kinases